Overview of the Genus Phyllactinia (Ascomycota, Erysiphales) in Azerbaijan

Plant & Fungal Research (2018) 1(1): 9-17

http://dx.doi.org/10.29228/plantfungalres.2
© The Institute of Botany, ANAS, Baku, Azerbaijan
December 2018

Overview of the genus Phyllactinia (Ascomycota, Erysiphales) in Azerbaijan

Dilzara N. Aghayeva¹Lamiya V. Abasova

Key Words: distribution, ectoparasitism, endoparasitism, host plant, plant pathogen, powdery mildews

Institute of Botany, Azerbaijan National Academy of Sciences, Badamdar 40, Baku, AZ1004, Azerbaijan

INTRODUCTION

Susumu Takamatsu

Powdery mildews are one of the frequently encoun-

tered plant pathogens and most of them are epiphytic (14 genera from 18), in which they tend to produce hyphae and reproductive structures on surface of leaves,

young shoots and inﬂorescence [Braun, Cook, 2012;

Glawe, 2008]. These fungi absorb nutrients from plant tissue via haustoria, which develops in epidermal cells

of plants [Braun, Cook, 2012]. Among all powdery mil-

dews only four genera demonstrate endoparasitism, of them Phyllactinia Lév., have partly endoparasitic na-

ture. Fungi belonging to these genera penetrate into the

plant cell via stomata and develop haustoria in parenchyma cells. Endoparasitic genera of powdery mildews

(Phyllactinia, Pleochaeta Sacc. & Speg., Queirozia

Viégas & Cardoso and Leveillula G. Arnaud) form a

distinct monophyletic group within Erysiphales which suggests that endoparasitism derived from ectoparasitism in powdery mildews only once in their evolution

[Takamatsu, 2013; Takamatsu et al. 2016]. Only genus

Leveillula exhibits true endoparasitism and elongates internal hyphae between host cells in mesophyll layer

[Takamatsu et al. 2008, 2016].

Phyllactinia is distinguishable from other powdery

mildews based on its unique characteristics of sexual

morphs, viz. large ascomata (chasmothecia) with two

different types of appendages. One of them is acicular

appendages with bulbous swellings at the base, which

arise equatorially and play role in orientation of asco-

mata through the air during dispersal. Second one, penicillate cells composed of foots (outgrows of the asco-

matal walls), ﬁlaments [Shin, Lee, 2002] and grouped together on the dorsal surface of chasmothecia [Glawe,

2008]. Penicillate cells perform a role as anchor for attaching of chasmothecia to the new plant surface by

gelatinizing of ﬁlaments under humid condition [Takamatsu et al., 2008]. There is a speculation that unique

characteristics of appendages are an evolutionary adap-

tation to the tree parasitism of this genus [Takamatsu

et al., 2008]. Powdery mildews from this genus form whitish to grayish colony under the leaf surface. The genus is characterized by having 2–3-spored asci, main-

Graduate School of Bioresources, Mie University, 1577 Kurima-Machiya, T s u 514-8507, Japan

Abstract: Intergeneric diversity of powdery mildews within the genus Phyllactinia in Azerbaijan was investigated using morphological approaches based on re-examination of herbarium specimens kept in Mycological Herbarium of the Institute of Botany (BAK), Azerbaijan National Academy of Sciences and collections of recent years. To contribute detail taxonomic analysis data given in literatures was revised. Modern taxonomic and nomenclature changes were considered. The host range and geographical distribution of species residing to the

genus within the country were clariﬁed. Consequently,

17 powdery mildew taxa were recorded, of which Ph.

alnicola, Ph. ampelopsidis, Ph. babayanii, Ph. carpini, Ph. corni, Ph. fraxini, Ph. guttata, Ph. mali, Ph. marissalii, Ph. moricola, Ph. nivea, Ph. orbicularis, Ph. paliuri, Ph. phaseolina, Ph. populi, Ph. pyri-serotinae

and Ph. roboris on 32 plant species from 11 families were listed. These families belong to the groups Aster-

ids (Cornaceae, Oleaceae) and Rosids (Fabaceae, Betulaceae, Fagaceae, Salicaceae, Moraceae, Rhamnaceae, Rosaceae, Ulmaceae, Sapindaceae, Vitaceae), of which Rosids exceeds in number of host species. The family Rosaceae possess the large amount of host species, but speciﬁc afﬁnity of genus Phyllactinia is considered to

be to the family Betulaceae. In addition, Phyllactinia powdery mildews seemed to spread mainly in mountainous areas of Azerbaijan. The highest number of taxa was recorded in the districts belonging to the Southern-

East Great Caucasus region of the country, followed by regions Middle Araz and Lesser Caucasus. The low-

est number of Phyllactinia taxa was recorded from Kur lowland and Lankaran regions. During the present study, it was revealed that herbarium samples of 14 taxa of genus Phyllactinia are available in the BAK, information of which is provided in this article.

Accepted for publication: 5 December 2018 ¹E-mail: [email protected]

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ly monomorphic, sometimes dimorphic conidia with clavate, dumble-like, subcylindric, broadly ellipsoidovoid, lanceolate shape, almost indistinct and nipple or

rod-shaped appressoria [Braun, Cook, 2012] (Fig. 1).

According to the monograph of the Erysiphales,
102 species were counted within the genus Phyllactinia

[Braun, Cook, 2012] and they are strictly woody para-

sitic fungi, which are known on about 700 plant species

from 69 families [Amano, 1986]. Totally, 108 plant species from family Rosaceae were dedected as host for

genus Phyllactinia and the order is followed by families

Betulaceae (91 species), Fagaceae (56 species), Oleaceae (50 species), etc. [Takamatsu et al., 2008].

The aims of this study were to reveal diversity of powdery mildews from the genus Phyllactinia, to clarify the ratio of Phyllactinia taxa within the Erysiphales in Azerbaijan, to update species composition by taking into the consideration modern taxonomic and nomenclature changes, and to investigate their host range and geographical distribution within country.

Figure 1. Phyllactinia moricola; A. acicular appendage

with bulbous swelling; B. penicillate cell, b1. foot, b2. ﬁlaments; C. conidia; D. conidiophores; E. appressoria; Bar = 100 μm.

MATERIAL AND METHODS
RESULTS AND DISCUSSION

Herbarium samples kept at the Mycological Herbarium of the Institute of Botany, ANAS (BAK) and new

samples collected from 2016 to 2018 were investigated

using classic morphological approaches. To contribute detail taxonomic investigations, literature data were summarized.
T a xonomy. Diversity of powdery mildews in Azerbaijan is currently represented with 134 fungal taxa from ten

genera on 420 plant species from 51 families [Abasova, Ağayeva, 2018]. The genus Erysiphe R. Hedw. ex DC.

dominates by possessing the largest number of fungal taxa, followed by the genus Podosphaera Kunze, Go-

lovinomyces (U.Braun) Heluta, Phyllactinia, and Lev- eillula. Genera Arthrocladiella Vassilkov, Blumeria Golovin ex Speer, Neoërysiphe U.Braun and Sawadaea

Miyabe are quite small and consist of one or two species for each genus [Abasova, Ağayeva, 2018]. Intergeneric

diversity of the genus Phyllactinia, their host range, geographical distribution within the country, and traditional names put on the specimens and BAK numbers of were given below.

Ph. alnicola U. Braun, Braun & Cook 226, 2012;

= Ph. suffulta f. alni Hammarl.; Host: Alnus glutinosa

(L.) Gaertn. (Betulaceae); BAK 5612, 5614, 5615; Distribution: Qusar, Zaqatala (Fig.2.1).

Ph. ampelopsidis Y.N. Yu & Y.Q. Lai, Acta Micro-

biol. Sin. 19 (1): 14, 1979; Host: Vitis vinifera L. (Vitaceae); BAK 5778; Distribution: Khojavend. Previ-

ously a powdery mildew fungus on Vitis vinifera from

Azerbaijan was described as Phyllactinia suffulta f. vi-

tis Jacz. [Huseynova, 1961a]. Herbarium specimen was

examined morphologically in this study, but not any other structure characterizing genus Phyllactinia was
Morphological examinations were done under the

optical microscope (Vert. A1, Carl Zeiss, Axio Imager,

Göttingen, Germany). To examine asexual structures a little piece of infected leaf was rehydrated using lactic

acid method [Shin, La, 1993]. For observation of sexual morphs, chasmothecia were mounted in 3% NaOH solution [Meeboon, Takamatsu, 2015]. Thirty measure-

ments for each structure were taken. Measurements of asexual structures were done based on the length of conidiophores, size and shape of conidia and appres-

soria. For sexual structures diameter of chasmothecia,

and number, size and shape of asci and ascospores were

considered. Bulmer’s factor (l × 1.5; w × 1.2) was used

to reconstruct the original size of conidia for herbarium

samples [Braun, Cook, 2012]. Drawings were made by

freehand using scale bar.

Identiﬁcation of fungal species was carried out by using the latest literature [Braun, Cook, 2012]. Nomen-

clature changes were done according to the Mycobank

and Index Fungorum. Systematic assignment of plants was performed based on APG IV system [APG IV, 2016].

10

Aghayeva et al.: The genus Phyllactinia in Azerbaijan

observed. Description of Ph. suffulta f. vitis provided

identiﬁed as Ph. fraxini.

by B. Huseynova is quite similar to those of Ph. ampelopsidis in 180–200 μm diameter of chasmothecia [in monograph 150–280 μm], 6–8 number [5–14] and up to 250 μm length [250–370 μm] of acicular appendages, 54–76 × 22–30 μm [50–100 × 20–45 μm] and ellipsoid-

ovoid, 2(–3)-spored of asci. However, Ph. suffulta f.

vitis was given the afﬁnity and status unclear taxa in monograph of the Erysiphales [Braun, Cook, 2012], but

this taxon was revised as Ph. ampelopsidis according to the description given in the literature. Additional col-

lections are required to clarify taxonomic status of this

species using molecular-phylogenetic and detail morphological approaches.

Ph. babayanii Simonyan, Mikol. Fitapatol. 18(6):

465, 1984; = Ph. salmonii f. amygdali Babayan; Host:

Prunus fenzliana Fritsch. (Rosaceae); BAK 5607; Dis-

tribution: Julfa.

Ph. carpini (Rabenh.) Fuss, Arch. Ver. Sibenb.

Landesk. 14(2): 463, 1878; = Ph. suffulta f. carpini- betuli Jacz.; Host: Carpinus betulus L. (Betulaceae);

BAK 5618–5623, 5627; Distribution: Qusar, Zaqatala,

Astara, Gadabay, Askeran.

Ph. guttata (Wallr.: Fr.) Lév., Bot., 3 Sér., 15: 144,

1851; ≡ Ph. corylea (Pers.) P.Karst.; = Ph. suffulta f. coryli-avellanae Jacz.; Host: Corylus avellana L., C.

colurna L. (Betulaceae); BAK 5597–5601, 5637–5645, 5648, 5650–5658; Distribution: Qusar, Khachmaz, Shabran, Shaki, Oghuz, Qakh, Zaqatala, Lankaran, Lerik, Shusha, Kalbajar, Askeran, Ordubad (Fig. 2.4).

Nowadays Erysiphe corylacearum U. Braun & S.

Takam. was recorded as a new powdery mildew pathogen on hazelnut in Azerbaijan and become well distrib-

ute here [Abasova et al., 2018]. However, both surface

of leaf, and nuts of hazelnut are became heavily infected by this pathogen, faint colonies of Ph. guttata also occur on the same leaves. Thus, now Ph. guttata coexists on the same host with E. corylacearum in the country.

Ph. mali (Duby) U. Braun, Feddes Repert. 88(9–
10): 657, 1978; ≡ Ph. mespili (Castagne) S. Blumer; =

Ph. suffulta f. pruni Jacz., f. piri Jacz.; = Ph. guttata f. crataegi-oxyacanthae Sacc.; Host: Crataegus meyeri A.Pojark, C. monogyna Jacq., C. orientalis M.Bieb., C. pentagyna Waldst. et Kit. ex Willd., Mespilus germani- ca L., Pyrus communis L., P . s alicifolia Pall., P . s yriaca Boiss., Cerasus microcarpa (C.A.Mey.) Boiss. (Rosa-

ceae); BAK 5602–5604, 5660, 5661, 5663, 5691–5697, 5702–5709, 5711, 5712, 10027; Distribution: Baku, Shabran, Quba, Qusar, Zaqatala, Qazakh, Khojavend, Lerik, Shusha, Ordubad, Shahbuz.
Ph. corni H.D.Shin & M.J.Park, Braun & Cook, 241,

2012; = Ph. suffulta f. corni Jacz.; Host: Cornus mas L.,

C. sanguinea L. (Cornaceae); BAK 5628–5632, 5634, 5635, 5636; Distribution: Zaqatala, Balakan, Askeran, Khojavend, Ordubad (Fig.2.2).
Ph. fraxini (DC.) Fuss, Arch. Ver. Siebenb. Landesk.

14(2): 463, 1878; Host: Fraxinus excelsior L., F . s og-

diana Bunge (Oleaceae); BAK 5667–5677, 5679; Distribution: Qusar, Khachmaz, Absheron, Zaqatala, Lerik, Shusha, Khojavend, Ordubad (Fig.2.3). Two Phyllac-

tinia species, Ph. fraxini and Ph. fraxinocola U.Braun

& H.D.Shin were known on Fraxinus spp. worldwide

[Braun, Cook, 2012]. According to the monograph of the Erysiphales [Braun, Cook, 2012] there is not major

differences in sexual morphs between these two species. Mainly they could be distinguished based on their

asexual structures [Scholler et al., 2018]. Specimens

namely Ph. suffulta f. fraxini DC. collected in Azer-

baijan were in sexual stage. Therefore identiﬁcation of

samples was done based on characteristics of sexual structures, principally on asci. Asci with 2–4-spors are

usual for both species, but 3–4-spored ones are frequent

in Ph. fraxini, which was observed in our specimens. Length of asci in our specimens varies between 70–101

μm, but it is 50–105 μm in Ph. fraxini and 50–90 μm in Ph. fraxinicola according to the Manual [Braun, Cook,

2012]. Based on these similarities our specimens were

Ph. marissalii (Westend.) U. Braun, Braun & Cook

262, 2012; = Ph. suffulta f. aceris Jacz.; Host: Acer

platanoides L. (Sapindaceae); Distribution: Oghuz, Zaqatala. Information about distribution of this fungus in

the country was given according in the Ibrahimov et al.

[1956]. But herbarium specimen of fungus was not deposited in BAK. New collections are needed to conﬁrm

distribution of this fungus in the country.
Ph. moricola (Henn.) Homma, Trans. Sapporo Nat.

Hist. Soc. 11: 174, 1930; = Ph. suffulta f. moricola Jacz.; Host: Morus alba L., M. australis Poir. (Morace-

ae); BAK 5605, 5680–5688, 5690, 10032; Distribution: Absheron, Zaqatala, Ordubad (Fig. 2.5).
Ph. nivea (Castagne) U. Braun, Braun & Cook 263,

2012; Host: Ulmus glabra Huds., U. minor Mill., U.

densa Litv. (Ulmaceae); BAK 5713–5717; Distribution: Khojavend, Ordubad, Babek (Fig. 2.6). Informa-

tion about distribution of this species in the country was

given in monograph of the Erysiphales [Braun, Cook,

2012]. But herbarium specimen of this fungus is not stored in BAK. While, samples of Phyllactinia fungus on Ulmus spp. collected in Azerbaijan were previously

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Plant & Fungal Research

identiﬁed as Ph. suffulta f. ulmi Jacz. and distribution

applicable for morphological examination and there is not any other additional collection to proof the status of this species. of this fungus within the country reported in numerous

local literature [Akhundov, 1965; Huseynova, 1961b; Ibrahimov et al., 1956]. Currently this taxon was re-

named as Ph. angulata var. ulmi U. Braun based on

modern taxonomic changes [Braun, Cook, 2012]. In

morphological re-analysis of specimens of Ph. sufful-

ta f. ulmi, clavate conidia in 33–72 × 18–22(–26) μm were observed. On whole, characteristics of sexual and

asexual morphs are in good agreement with Ph. nivea

by having clavate, 50–70 × 15–22 μm conidia [Braun,

Cook, 2012]. Whereas Ph. angulata var. ulmi is char-

acterized by its unique shape of conidia (dumb-bell-

shape), which was not found in our specimens. Therefore, specimens previously reported as Ph. suffulta f.

ulmi were re-identiﬁed as Ph. nivea.

Ph. populi (Jacz.) Y.N.Yu, in Yu & Lai, Acta Micro-

biol. Sin. 19(1): 18, 1979; = Ph. suffulta f. populi Jacz.;

Host: Populus sp. L. (Salicaceae); Distribution: Quba, Zaqatala. Morphological description and information

about distribution of this species were given according

to the local literature [Ibrahimov et al., 1956]. However,

herbarium specimen was not deposited to BAK.

Ph. pyri-serotinae Sawada, Rep. Dept. Agric.

Gov. Res. Inst. Formosa 49:83, 1930; =Ph. suffulta

f. cotoneastri Jacz.; Host: Cotoneaster racemiﬂorus

(Desf.) C.Koch. (Rosaceae); BAK 5659; Distribution:

Shahbuz.

Ph. roboris (Gachet) S. Blumer, Beitr. Krypt-Fl.
Schweiz 7(1): 389, 193; Host: Quercus iberica M.Bieb., Q. robur L. (Fagaceae); BAK 5606, 5616, Distribution:

Shusha, Ganja. Distribution of Ph. roboris on oak spe-

cies in Azerbaijan was mentioned by Huseynov [Huseynov, 1988]. Fungus was collected in asexual stage from

Ganja district. Besides, information about powdery

mildew belonging to the genus Phyllactinia on Quercus spp., which was identiﬁed as Ph. suffulta var. angulata

(E.S. Salmon) Sacc. & Trotter given in some local man-

uscripts [Huseynova 1961 a, b]. This fungus is men-

tioned as Ph. angulata (E.S. Salmon) S. Blumer var.

angulata in Index Fungorum and this species is char-

acterized by having dumb-bell-shaped conidia and endemic to North America. Two specimens of Ph. suffulta var. angulata were revised morphologically. Herbarium

sample (BAK 5617) collected from Khojavend district was re-examined and was identiﬁed as E. alphitoides (Griff. & Maubl.) U. Braun & S. Takam.
Specimen (BAK 5616) collected from Shusha was

in sexual stage and conidia were not found to proof the taxonomic status of this species. Thus, the specimens of

Ph. suffulta var. angulata were re-named as Ph. roboris.

Thereby, the sum of Phyllactinia powdery mildews occupies 13% of all powdery mildew species in this coun-

try (Fig. 3), which is a little bit higher compared with the percentage in the world (10%) (Fig. 4).
Ph. orbicularis (Ehrenb.) U. Braun, Braun & Cook
264, 2012; Host: Fagus orientalis L. (Fagaceae); BAK 5665; Distribution: Zaqatala (Fig. 2.7). Ph. suffulta f.

fagi Duby was known on beech trees in Azerbaijan to

date [Ibrahimov, 1956]. Information of this taxa was found neither in monograph of the Erysiphales [Braun, Cook, 2012], nor in Index Fungorum. According to the

morphological re-examination of specimen of Ph. suf-

fulta f. fagi, fungus was revised as Ph. orbicularis based

on identity of sexual morphs in 150–190 μm diam. of chasmothecia [175–265 μm]; 6–12 [4–18] number of acicular appendages; 54–72 × 26–30 μm size [(50–)60– 95 × 25–45 μm] and having 2-spored asci.
Ph. paliuri U. Braun, Braun & Cook, 265, 2012;

Host: Paliurus spina-christi Mill. (Rhamnaceae); BAK

5699, 5700; Distribution: Oghuz, Lankaran, Astara

(Fig. 2.8). Phyllactinia powdery mildew fungus on

thorn plants was reported as Ph. suffulta f. paliuri Sacc.

in Azerbaijan, so far [Ibrahimov et al., 1956]. In Monograph [Braun, Cook, 2012] and Index Fungorum this

taxa was not mentioned. The fungus from specimens of

Ph. suffulta f. paliuri was re-identiﬁed as Ph. paliuri

according to the morphological analysis.
Ph. phaseolina N. Ahmad, D.G. Agarwal & A.K.

Sarbhoy, Mycotaxon 29: 68, 1987; =? Ph. suffulta f.

viciae Guseinova; Host: Vicia sepium L. (Fabaceae);

BAK 5719; Distribution: Shusha. Fungi from the ge-

nus Phyllactinia are known as strictly woody parasitic

plant pathogens worldwide. However, fungus was ﬁrst

described on herbaceous plant (V . s epium) as Ph. suf-

fulta f. viciae in Azerbaijan [Huseynova, 1961] and cur-

rently was renamed as Ph. phaseolina based on modern

taxonomic changes [Braun, Cook, 2012]. This species

is considered as doubtful, due to the type material is not
Host range. In the current study, 32 plant species from 12 families were recorded as hosts for the genus Phyllactinia in Azerbaijan. This is only 5% of total number of host plants for this genus in the world.

These families allocated among Asterids (Cornaceae, Oleaceae) and Rosids (Fabaceae, Betulaceae, Fagaceae, Salicaceae, Moraceae, Rhamnaceae, Rosaceae, Ulma-

ceae, Sapindaceae, Vitaceae) groups. Economically im-
12

Aghayeva et al.: The genus Phyllactinia in Azerbaijan

Figure 2.1. Phyllactinia alnicola on Alnus glutinosa (BAK 5612): A. chasmothecia; B,C. asci and ascospores; 2.2.

Ph. corni on Cornus mas (BAK 5630): A. chasmothecia; B,C. asci and ascospores; 2.3. Ph. fraxini on Fraxinus excelsior (BAK 5670): A. chasmothecia; B, C. asci and ascospores; 2.4. Ph. guttata on Corylus avellana (BAK

5645): A. chasmothecia; B. ascus and ascospores; C. penicillate cells; 2.5. Ph. moricola on Morus australis (BAK 5685): A. chasmothecia; B, C. asci and ascospores; 2.6. Ph. nivea on Ulmus minor (BAK 5713): A. chasmothecia; B. ascus and ascospores; C. penicillate cells; 2.7. Ph. orbicularis on Fagus orientalis (BAK 5665): A. chasmothecia, B. acicular appendages with bulbous swelling; C. penicillate cells; D. asci and ascospores; 2.8. Ph. paliuri on Paliurus spina-christi (BAK 5700): A. ruptured casmothecia; B. acicular appendage with bulbous swelling; C, D, E. asci and ascospores; Bar = 100 μm.